Skip to main content
Log in

Autotrophic starch production by Chlamydomonas species

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Microalgal autotrophic cultures may be used as starch feedstocks for a wide spectrum of food and non-food applications, starch-based plastics production included. Chlamydomonas is known to accumulate carbohydrates, but only Chlamydomonas reinhardtii is widely studied. This is the first paper that analyzes the starch content and production rate of four non-conventional Chlamydomonas species and compares their performances to the benchmark C. reinhardtii. Two culture systems—shaken flasks and inclined bubble column (IBC) photobioreactors—and nitrogen depletion conditions were characterized. The irradiance was set at 95 μmol photons m−2 s−1 for flask system and at 220 μmol photons m−2 s−1 for photobioreactors. CO2 and light depletion in shaken flasks strongly affected growth rate and starch production. Under these limiting condition, Chlamydomonas applanata had the best starch productivity of 1.2 mg L−1 day−1. In IBC photobioreactors, the microalgal growth rate and starch production improved with respect to the flask system and nitrogen depletion promoted starch accumulation. The best results of starch productivity and maximum starch fraction were 53 mg L−1 day−1 and 45%DW for Chlamydomonas oblonga and Chlamydomonas moewusii, respectively. This was 49 % more than the studied benchmark. A fast and simple method for starch localization in the microalgal cells was also proposed. The starch granules surrounded the pyrenoid under the growth phase, while they fill the whole cell under nutrient depletion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abou-Shanab RAI, Matter IA, Kim SN, Oh YK, Choi J, Jeon BH (2011) Characterization and identification of lipid-producing microalgae species isolated from a freshwater lake. Biomass Bioenergy 35:3079–3085

    Article  CAS  Google Scholar 

  • Bafana A (2013) Characterization and optimization of production of exopolysaccharide from Chlamydomonas reinhardtii. Carbohyd Polym 20:746–752

    Article  Google Scholar 

  • Barsanti L, Frassanito AM, Passarelli V, Evangelista V (2013) Tetraflagellochloris mauritanica gen. et sp. nov. (Chlorophycae), a new flagellated alga from the Mauritanian Desert: morphology, ultrastructure, and phylogenetic framing. J Phycol 49:178–193

    Article  CAS  PubMed  Google Scholar 

  • Brányiková I, Maršálková B, Doucha J, Brányik T, Bisovà K, Zachleder V, Vitovà M (2011) Microalgae-novel highly efficient starch producers. Biotechnol Bioeng 108:766–776

    Article  PubMed  Google Scholar 

  • Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffells RH (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226

    Article  CAS  PubMed  Google Scholar 

  • Breuer G, De Jaeger L, Artus VPG, Martens DE, Draaisma RB, Wijffells RH (2014) Superior triacylglycerol (TAG) accumulation in starchless mutants of Scenedesmus obliquus: evaluation of TAG yield and productivity in controlled photobioreactors. Biotechnol Biofuels 7:70–82

    Article  PubMed  PubMed Central  Google Scholar 

  • Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331

    Article  CAS  Google Scholar 

  • Buléon A, Colonna P, Planchot V, Ball S (1998) Starch granules: structure and biosynthesis. Int J Biol Macromol 23:85–112

    Article  PubMed  Google Scholar 

  • Busi MV, Barchiesi J, Martin M, Gomez-Casati DF (2014) Starch metabolism in green algae. Starch 66:28–40

    Article  CAS  Google Scholar 

  • Chen CY, Zhao XQ, Yen HW, Ho SH, Cheng C-L, Lee DJ, Bai F-W, Chang JS (2013) Microalgae-based carbohydrates for biofuel production. Biochem Eng J 78:1–10

    Article  CAS  Google Scholar 

  • Collos Y, Mornet F, Sciandra A, Waser N, Larson A, Harrison PJ (1999) An optical method for the rapid measurement of micromolar concentrations of nitrate in marine phytoplankton cultures. JAppl Phycol 11:179–184

    Article  Google Scholar 

  • Demchenko E, Mikhailyuk T, Coleman AW, Pröschold T (2012) Generic and species concepts in Microglena (previously the Chlamydomonas monadina group) revised using an integrative approach. Eur J Phycol 47:264–290

  • Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Ener 88:3331–3335

    Article  CAS  Google Scholar 

  • Fernandes B, Teixeira J, Dragone G, Vicente AA, Kawano S, Bisovà K, Pribyl P, Zachleder V, Vitovà M (2013) Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresour Technol 144:268–274

    Article  CAS  PubMed  Google Scholar 

  • Gargano I, Olivieri G, Andreozzi R, Marotta R, Marzocchella A, Pinto G, Pollio A (2013) Effects of photobioreactor depth on Stichococcus cultures aimed at biodiesel production. Chem Eng Trans 32:1117–1122

    Google Scholar 

  • Gorelova O, Baulina O, Solovchenko A, Selyakh I, Chiukunova O, Semenova L, Scherbakov P, Burakova O, Lobakova E (2015) Coordinated rearrangements of assimilatory and storage cell compartments in a nitrogen-starving symbiotic chlorophyte cultivated under high light. Arch Microbiol 197:181–195

    Article  CAS  PubMed  Google Scholar 

  • Ho SH, Chen CY, Chang JS (2012) Effect of light intensity and nitrogen starvationon CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113:244–252

    Article  CAS  PubMed  Google Scholar 

  • Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryotic Cell 12:776–793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamalanathan M, Pierangelini M, Shearman LA, Gleadow R, Beardall J (2016) Impacts of nitrogen and phosphorus starvation on the physiology of Chlamydomonas reinhardtii. J Appl Phycol 28:1509–1520

    Article  CAS  Google Scholar 

  • Khalil ZI, Asker MS, El-Sayed S, Kobbia IA (2010) Effect of pH on growth and biochemical responses of Dunaliella bardawil and Chlorella ellipsoidea. World J Microbiol Biotechnol 26:1225–1231

    Article  CAS  PubMed  Google Scholar 

  • Kliphuis AMJ, Klok AJ, Martens DE, Lamers PP, Janssen M, Wijffles RH (2012) Metabolic modeling of Chlamydomonas reinhardtii: energy requirements for photoautotrophic growth and maintenance. J Appl Phycol 24:253–266

    Article  CAS  PubMed  Google Scholar 

  • LMC International Ldt (2002) Evaluation of the community policy for starch and starch products. Prepared for: European Commission – DG Agriculture Rue de la Loi 200/Wetstraat 200 B-1049 Bruxelles/Brussel

  • Meuser JE, Ananyev G, Wittiga LE, Kosourovc S, Ghirardi ML, Seibert M, Dismukes GC, Posewitz MC (2009) Phenotypic diversity of hydrogen production in chlorophycean algae reflects distinct anaerobic metabolisms. J Biotechnol 142:21–30

    Article  CAS  PubMed  Google Scholar 

  • Miller BJN (2010) Food analysis. Nielsen SS, 4th edn. Springer, New York

  • Moheimani NR, Borowitzka MA (2006) The long-term culture of the coccolithophore Pleurochrysis carterae (Haptophyta) in outdoor raceway ponds. J Appl Phycol 18:703–712

  • Msanne J, Xu D, Konda AR, Casas-Mollano JA, Awada T, Cahoon EB, Cerrutti H (2012) Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 75:50–59

    Article  CAS  PubMed  Google Scholar 

  • Muller T, Bleiss W, Martin C-D, Rogaschewski S, Fuhr G (1998) Snow algae from northwest Svalbard: their identification, distribution, pigment and nutrient content. Polar Biol 20:14–32

    Article  Google Scholar 

  • Nascimento IA, Marques SSI, Cabanelas ITD, Pereira SA, Druzian JI, de Suoza CO, Vich DV, de Carvalho GC, Nascimento MA (2013) Screening microalgae strain for biodiesel production: lipid productivity and estimation of fuel quality based on fatty acids profiles as selective criteria. Bioenergy Res 6:1–13

    Article  CAS  Google Scholar 

  • Olivieri G, Gargano I, Andreozzi R, Marotta R, Marzocchella A, Pinto G, Pollio A (2013) Effects of photobioreactors design and operating conditions on Stichococcus bacillaris biomass and biodiesel production. Biochem Eng J 74:8–14

    Article  CAS  Google Scholar 

  • Pollio A, Cennamo P, Ciniglia C, De Stefano M, Pinto G, Huss VA (2005) Chlamydomonas pitschmannii Ettl, a little known species from thermoacidic environments. Protist 156:287–302.

  • Renaud SM, Thinh LV, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch culture. Acquaculture 211:195–214

    Article  CAS  Google Scholar 

  • Schulze K, Lòpez DA, Tillich UM, Frohme M (2011) A simple viability analysis for unicellular cyanobacteria using a new autofluorescence assay, automated microscopy, and Image J. BMC Biotechnol 11:118–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7–22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srinivas T (2007) Industrial demand for cassava starch in India. Starch 59:477–481

    Article  CAS  Google Scholar 

  • Tanadul O, Vandergheynst JS, Beckles DM, Powell ALT, Labavitch JM (2014) The impact of elevated CO2 concentration on the quality of algal starch as a potential biofuel feedstock. Biotechnol Bioeng 111:1323–1331

    Article  CAS  PubMed  Google Scholar 

  • Yao C, Ai J, Cao X, Xue S, Zhang W (2012) Enhancing starch production of marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresour Technol 118:438–444

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the Regione Campania (Italy) for the financial support to the project P.O.R. FESR 2007/2013 BioIndustrial Processes—BIP (CUPB25C13000290007).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Olivieri.

Electronic supplementary material

Fig. S1

(DOCX 88 kb)

Fig. S2

(DOCX 2388 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gifuni, I., Olivieri, G., Pollio, A. et al. Autotrophic starch production by Chlamydomonas species. J Appl Phycol 29, 105–114 (2017). https://doi.org/10.1007/s10811-016-0932-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0932-2

Keywords

Navigation